Topographically distinct visual and olfactory inputs to the mushroom body in the Swallowtail butterfly,Papilio xuthus

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Abstract

Papilio

butterflies depend highly on visual information in their flower-foraging behavior. The retina of Papilio xuthus has been studied well, whereas the visual system in the brain is poorly understood. By investigating outputs from the optic lobe to the central brain, we found that the mushroom body of P. xuthus receives prominent direct inputs from the optic lobe in addition to olfactory inputs. The mushroom body consists of three components: the calyx, the pedunculus, and the lobes. The calyx is further subdivided into two cup-shaped primary calyces and an accessory calyx. Each primary calyx consists of three concentric subareas, the inner zone, the outer zone, and the rim of the outer zone. Dextran injections into the optic lobe, the calyx, or the antennal lobe revealed three visual inputs and one olfactory input into the calyx. The visual inputs originate from the medulla, the lobula, and a newly identified neuropil, the ventral lobe of the lobula. All visual inputs first innervate the accessory calyx, and the two lobula inputs further spread their processes through the inner zone and the rim of the outer zone of the primary calyces. Visual inputs from the medulla and the ventral lobe of the lobula collect light information from ventral eye regions, suggesting a role in visual target detection rather than sky compass orientation. In contrast to visual inputs, olfactory inputs innervate only the calycal outer zone. The multisensory inputs to the mushroom bodies in P. xuthus are probably related to their flower-foraging behavior. J. Comp. Neurol. 523:162–182, 2015. © 2014 Wiley Periodicals, Inc.

Three visual inputs from the medulla (red), the lobula (yellow) or the ventral lobe of the lobula (orange) are determined in the calyces of the mushroom body by dextran injection. In calyx, these visual inputs (dark orange) are clearly segregated from the olfactory input (blue).

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